jear2012 [Journal of Entomological and Acarological Research 2023; 55:10861] [page 1] Abstract Despite their potential as indicators of water quality and their key role in river ecosystems, Chironomidae is still poorly studied in Neotropical rivers. This lack of knowledge is especially rele- vant for rivers subjected to intense human activities, such as many rivers in Mexico. The aim of this investigation is to contribute to the knowledge of the midges of the Pesquería River (Mexico) along its main courses and relate the composition and abundance to river health. Thirty samples were collected during two different periods (August 2015 and February 2016) using a D-frame and kick sampling. Thirty-five taxa were found in total, with four taxa found in more than 50% of the sites and 19 only found once. Midges accounted for more than 50% of the total macroinverte- brate abundance. Chironomus gr. plumosus, Rheotanytarsus spp. and Cricotopus gr. bicinctus were the most abundant species. Collector-gatherers dominated in August (71% of individuals), whereas collector-filterers dominated in February (43,2%). The major factor explaining the midge distribution and abundance is pollution, while the structure of riparian area does not explain much of the midge richness. This is most likely related to the organic pollution coming from untreated or poorly treated sewage in the city of Monterrey and its surroundings. Three main sectors are distinguished along the river: i) the upper part section with higher biodiversity and presence of intolerant taxa; ii) the middle sewage polluted area with the presence of large red midges very tolerant to pollution (Chironomus, Dicrotendipes); iii) the lower section in the agricultural zone where the community is dominated by red, small midges (Rheotanytarsus). Overall, our study shows that Chironomidae can be useful as better indicators of water qual- ity when genera or species levels are used instead of family or subfamily, as is usually found in most papers on river pollution. Introduction Midges are an important component of river life. At some sites Chironomidae larvae comprise an important percentage of the total density and biomass of aquatic macroinvertebrates and they can be an important component of the diet of fishes and other predators (Armitage et al., 1995). They can even significantly contribute to the terrestrial organic matter budget of riparian areas by exporting flying adults (Soininen et al., 2015). However, the taxonomic classification of midges is difficult and time-consum- ing (Andersen et al., 2013). Thereby, midges are usually identified only at the family level in ecological studies and water quality assessments and are considered to be pollution-resistant taxa and collector-gatherers as a trophic group (Armitage et al., 1995). However, they comprise a great variety of species covering a wide range of pollution tolerance. Thus, the taxonomic level at which midges are identified is very important (Edward et al., 2000; Molineri et al., 2020). The use of genera, species groups, or species (when possible) can help to reveal ecological patterns and Journal of Entomological and Acarological Research 2012; volume 44:eJournal of Entomological and Acarological Research 2023; volume 55:10861 INSECT ECOLOGY Chironomidae as indicators of water pollution in Pesquería River (México) Narcís Prat, Daniel Castro-López F.E.M. Research Group (Freshwater Ecology Management), Departament de Biología Evolutiva, Ecologia i Ciències Ambientals, Sección Ecología, Universitat de Barcelona, Barcelona, Spain Correspondence: Narcís Prat, F.E.M. Research Group (Freshwater Ecology Management), Departament de Biología Evolutiva, Ecologia i Ciències Ambientals. Sección Ecología. Universitat de Barcelona, diag- onal 645, 08028, Barcelona, Spain. Tel.: +34.934037135/607074784. E-mail: nprat@ub.edu Key words: midges; pollution; biomonitoring; aquatic macroinverte- brates; wastewater; functional feeding groups. Acknowledgments: the authors are grateful to the Civil Engineering Institute and the International Water Centre of the Universidad Autónoma de Nuevo Léon for helping in field and laboratory work. Thanks to Miguel Cañedo-Argüelles for English improvement and comments to the text. Contributions: NP, conceived the paper, identified midges, wrote the paper; DCL, field work, sort and classification of macroinvertebrates until family and help in the writing. All the authors approved the final version to be published. Conflict of interest: the authors declare no potential conflict of interest. Funding: Centro Internacional del Agua, Facultad Ingenieria Civil, Universidad Autónoma de Nuevo León. Received: 25 October 2022. Accepted: 22 March 2023. Publisher’s note: all claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organi- zations, or those of the publisher, the editors and the reviewers. Any prod- uct that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher. ©Copyright: the Author(s), 2023 Licensee PAGEPress, Italy Journal of Entomological and Acarological Research 2023; 55:10861 doi:10.4081/jear.2023.10861 This article is distributed under the terms of the Creative Commons Attribution-NonCommercial International License (CC BY-NC 4.0) which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. No n- co mm er cia l u se on ly [page 2] [Journal of Entomological and Acarological Research 2023; 55:10861] processes (e.g., Puntí et al., 2009; Cañedo-Argüelles et al., 2016; González-Trujillo et al., 2019). Usually, environmental factors explain most of the differences in the chironomid assemblage composition (e.g., Nicacio & Juen, 2018), although dispersal limitations might be important depend- ing on the network connectivity (Cañedo-Argüelles et al., 2015) and the temporal (Cañedo-Argüelles et al., 2020) and spatial scales considered (Viana & Chase, 2020). Micro-scale study of substrate composition and temporal changes between seasons and years may explain the coexistence of many species in the same site, but species level is necessary to detect such differences (Prat & Garcia-Roger, 2018). The Chironomidae of Mexico are still poorly known (Bello- González et al., 2019); a taxa list is available by Spies & Reiss, 1996, mostly from old papers. As Mexico shares part of its territory with Neotropical and Nearctic regions, the study of midges is more complex in this region. No specific keys exist for midges of Mexico; larvae are classified using the keys of Ferrington et al., (2008) and Epler (2001) for Nearctic fauna. For the Neotropical region, the key of Da Silva et al., (2018) is useful. But there is still a long way to arrive at a good understanding of the taxonomy, bio- geography, richness, and ecology of Mexican Chironomidae. Mexican rivers are subjected to great pressure. Despite that CONABIO (National Commission for the Understanding and Usage of Biodiversity) implemented the Priority Hydrological Regions (RHP) program in 1998 (Arriaga et al., 2009), their eco- logical degradation is increasing year after year. The program con- siders the Pesquería River (Nuevo Léon, México) as a priority case for ecological evaluation. Recent studies on this river showed that it is heavily impacted along most of its catchment, and a few sites are in good ecological status (Castro-López et al., 2019a, b). Despite recent efforts to consider biological communities (Torres-Olmera et al., 2018), water quality assessment currently relies exclusively on physicochemical parameters in Mexico. However there are several macroinvertebrate-based biological indices in Mexico (e.g., Perez-Munguia & Pineda-López, 2005), but most of them use a limited taxonomical knowledge (Family) (e.g., Carmona-Jiménez & Caro-Borrero, 2017), also in biomoni- toring studies (Castillo et al., 2018). Only a few studies regarding Paleolimnology (Pérez et al., 2013) or focusing on epiphytic midges (Caro-Borrero, A. & Carmona-Jiménez, J. 2018) have explored the use of genera or species-level. The aim of this investigation was to contribute to the knowl- edge of midges in the Pesquería River (Mexico) along its main course and to assess their potential as indicators of river health. The specific objectives of the study were to: i) characterise the bio- diversity of Chironomidae in the Pesquería River; ii) assess the relationship of Chironomidae communities with river health; iii) discuss the potential of Chironomidae to be used as bioindicators in Mexican rivers and streams. Materials and Methods Study area This study was conducted in The Pesquería River located in Northeastern Mexico (San Juan River Basin, at the coordinates 26º38’24”-25º26’24” latitude N and 100º54’00”-98º56’24” longi- tude W). The main stem flows through Monterrey city metropoli- tan area. The river has an average gradient of 0.4%, a length of 288.22 km and an area of 5255.56 km2, with an annual average flow of 2,04 m3/s (Ferriño, 2016). The section studied consisted of the last 108 km of the main course and comprised altitudes ranging between 104 and 542 m. a.s.l. The climate in the area is semi-arid to arid. The wet season occurs during the months of May to October, while the dry season occurs during the remaining months (November to April) (Castro-López et al., 2019) Sampling We sampled Chironomidae on two occasions (August 2015 and February 2016) at 15 sites. The location of stations along the river is in Figure 1 from Castro-López et al., (2019b). Macroinvertebrate samples were taken using a D-frame net (250 um mesh), in a 100 m reach. 20 kick samples were taken propor- tionally to the habitats present and combined in a unique sample. We preserved samples in 10% formalin and transported them to the laboratory. Initially, we identified macroinvertebrates at different taxonomic levels but midges only at the family level (Castro- López et al., 2019b). During the sorting, we pooled midges togeth- er in a tube and preserved them in 70% ethanol until the moment of their examination for taxonomical purposes. We studied a total number of 1670 and 1723 individuals for each season. The midges were classified using a two-step process. First, we classified midges into morphotypes under a stereoscope at x20. We used color, the presence of body setae, and others for distinguish- ing morphotypes following the criteria of Prat et al. (2012) and Rossaro et al., 2022a. With this approach, several genera o even species groups are easily recognized. When the morphotypes were not enough for identifying a genera or species group, we mounted 10 individuals of each morphotype to be identified using a micro- scope and following Epler (2001). Instead of Euparal, we use DMXF as mounting media because no dehydration was necessary. We identified the larvae using the keys of Epler (2001), Andersen et al. (2013), Ferrington et al. (2008), and Prat et al. (2012). We used the material from the collection of the senior author (N. Prat) for comparison. Genera or species groups are the result of such work, which is enough for the purposes of this paper and relevant for ecological studies (Molineri et al., 2020). We measured the status of riparian areas with the índex QBR adapted for the Pesquería River (QBR-RNMX in Castro-López et al., 2019a) from the original índex described in Munné et al. (2003). Data treatment The assignment of Chironomidae to a trophic group was made according to the categories used in Castro-López et al. (2019): predators, shredders, herbivores, collector-gatherers, and collector- filterers. Usually, midges were considered as collectors gatherers Article Figure 1. Relationship between QBR and number of taxa of midges. No n- co mm er cia l u se on ly in many studies. However, there are different feeding strategies within the Chironomidae genera or species (Serra et al., 2015, Caleño-Ruiz, 2015; Rodriguez-Lozano et al., 2015). We used our knowledge and personal observations on gut contents of midges from Pesqueria, to assign to each genus a trophic category. Results Environmental data Environmental data, the extent, and characteristics of the land cover are provided in previous papers (Castro-López et al., 2019a, 2019b). We distinguish three areas along the river (Table 1). The upper part area, before the urban metropolitan area of Monterrey (sites 1-3). Here, most of the basin cover is a mixed forest or shrub- land that extends until the riparian area, while water is mesohaline according to the geology of the area. In the middle area, the urban sprawl of Monterrey dominates, and the riparian area is mostly devoid of vegetation. In this section, six sewage plants and several unthreatened discharges discharge along the river, with a very large increase in values of conductivity and lower values of oxygen. Finally, in the final part of the river, after Monterrey, orchards dominated, both in the basin and in the riparian area. Conductivity is lower, and oxygen recovers, but pollution from sewage plants remains. We will use this river delimitation, previously defined by Castro-López et al., 2019a, to compare changes in the composition and abundance of midges. Number of taxa 35 Chironomidae taxa were found, 31 in August 2015 and 29 in February 2016 (Supplementary Material). The number of midge taxa per site ranged between 1 and 16 in August and between 2 and 14 in February. Nineteen taxa in August and 17 in February were rare (recorded in less than 2 samples). Only 7 taxa in August and 3 in February were present at more than 50% of the sites. Seven of the taxa were found only in August, and four only in February. In August, the headwater sites (1-4) accounted for most of the species richness, whereas on February 6 sites captured most of the taxa (Figure 2). Composition and relative abundance Chironomidae was present in all samples, and its total abun- dance was close to 50% of the macroinvertebrates found in both seasons (Table 2). The most frequent and abundant taxa were the same on both dates (Table 3): Rheotanytarsus spp., Chironomus gr. plumosus, Cricotopus gr. bicintus and Thienemannimyia sp. While Ch. gr plumosus dominated in August (up to 50% of the individu- als), Rheotanytarsus (42%) was in February. [Journal of Entomological and Acarological Research 2023; 55:10861] [page 3] Article Figure 2. Accumulated number of taxa of Chironomidae in the two seasons studied in the Pesquería River (Mexico). Table 1. Riparian uses and values of conductivity in the three main sections of the Pesqueria-River (data from Castro-López et al., 2019a). % Riparian Use Natural Urban Agricultural Sites 1-3 73-100 0-27 0 Sites 4-9 0 100 0 Sites 10-16 0-39 0 41-100 Conductivity 1758 (44) 5272 (1008) 2187 (116) Table 2. Most frequent and relatively abundant taxa of macroinvertebrates in Pesquería River (México) (data from Castro-López et al., 2019). August February Macroinvertebrates Sites (n=16) % Sites (n=16) % Chironomidae (cg) 16 48.38 15 54.53 Hyalella (cg) 7 18.78 8 12.06 Oligochaeta (cg) 14 14.71 16 15.96 Notodromidae (cg) 10 6.13 15 3.87 Smicridea (cf) 11 3.17 1 1.69 Simulinii (cf) 6 0.27 11 4.06 Nehalennia (p) 11 0.18 10 0.11 Enallagama (p) 11 0.15 11 0.11 Ceratopogonidae (p) 11 1.6 6 0.16 Argia (p) 11 0.27 12 0.37 Agraylea (h) 10 0.65 10 0.36 p, predator; h, herbivore; cg, collector gatherer; cf, collector-filterer. No n- co mm er cia l u se on ly [page 4] [Journal of Entomological and Acarological Research 2023; 55:10861] In polluted parts (below sewage plants, sites 9 and 10) Chironomus were present and abundant together with Polypedilum gr. halterale (see Annex 1). Only in sites 1 to 3 (upstream) and 16 and 17 (downstream), the four most abundant taxa were not dom- inant in both sampling periods. Most of the “rare species” are pres- ent in these 4 sites, while impacted sites usually have lower rich- ness and higher abundances of common species with red color (with hemoglobin). However, large community differences exist between sites 1-3 (upstream) and 16-17. The last ones have domi- nance of some pollution-tolerant species (like Dicrotendipes gr fumidus or Rheotanytarsus), while these are scarce in less dis- turbed sites of the headwaters of the river. Functional feeding groups According to the previous studies (Castro-López et al., 2019a) and personal observations from gut contents, the most common midges in Pesquería River are collector-gatherers and collector fil- terers (Tables 3, 4). As we can see in Table 3, the collector-gather- ers dominate in the first sampling season and collector filterers in February. This is coincident with the dominance of the different subfam- ilies of Chironomidae, as can be seen in Table 5, where Chironominae (Chironomus and Dicrotendipes) dominated in the first season and Tanytarsinii (Rheotanytarsus) in the second. The predators are members of the subfamily Tanypodinae and represent close to 10% of the individuals usually. Orthocladiinae are the more abundant subfamily within the herbivores. The importance of riparian area for midge composition and abundance In the upper part of the river, QBR-RNMX is high or very high (70-100). Values may be very low (sites 4-5-6) or high (up to 70 in sites 7-8). In the most polluted sites, QBR is lower than 50 (sites 9-10), with some recovery afterward in the agricultural zone, where the index is closer to or higher than 70. More details about the QBR and its importance in the Pesquería River are in Castro- López et al. (2019a). There is no direct relationship between the values of QBR- RNMX and the number of taxa of midges (Fig. 2). High values of both indexes upstream, while in the urban area taxa richness is low, but QBR may be variable because, although the river flows into Article Table 3. Most common and abundant Chironomidae of Pesquería River in the two seasons studied. August February Chironomidae Sites (n=16) % Sites (n=16) % Larsia (p) 8 2.8 6 2.6 Thienemanninyia (p) 9 4.6 10 5.3 Thienemanniella (h) 6 1.9 5 1.6 Cricotopus gr. bicinctus (h) 8 6.3 7 13 Chironomus gr. plumosus (cg) 10 56 6 19 Dicrotendipes gr. fumidus (cg) 9 5.7 5 7.4 Polypedilum gr. halterale (cg) 9 8.9 3 0.8 Rheotanytarsus (cf) 9 2.4 10 42 p, predator; h, herbivore; cg, collector gatherer; cf, collector-filterer. Table 4. Percentage of individuals of midges in each functional feeding group, in Pesquería River (categories of each taxon in Table 2). Functional feeding groups August February Predators 11.3 10 Herbivores 12.2 15.8 Collectors-gatherers 71.8 31 Collectors-filterers 4.6 43.2 Table 5. Changes in the frequency of appearance and dominance in the subfamilies of Chironomidae in the Pesquería River in two differ- ent seasons. Subfamilies August February of Chironomidae Sites % Sites % Tanypodinae 14 9.58 14 9.29 Orthocladiinae 12 10.90 9 15.79 Chironominae 15 79.52 15 74.93 Chironominii 15 73.35 14 31.40 Pseudochironominii 3 1.80 4 0.70 Tanytarsinii 11 4.37 12 42.83 Total 15 100 15 100 No n- co mm er cia l u se on ly densely populated area, some stretches still have patches of remnant riparian forests, where QBR-RNMX may be high. In the agricultur- al zones (sites 13-15), the values of QBR recover (up to 85) but not the richness of midges. No relationships exist with the midge troph- ic group or the QBR-RNMX (data not shown). These results are in concordance with those of Castro-López et al. (2019a), which also conclude that no relationships existed between the landscape, ripar- ian characteristics, and freshwater macroinvertebrates. Relationships with pollution We use the three-river sectors from Table 1 to explore the rela- tionships between pollution and midges. The upper less polluted part had lower values of conductivity (below 2000 uS/cm), high oxygen content (>8mg/l), and no inputs from sewage plants or urban effluents and is the more biodiverse area. High-polluted sites are in the Monterrey urban area, especially after the inputs of the 6 sewage plants, where oxygen can be extremely low, salinities high- er, and plenty of organic matter. The river's lower part, surrounded by agricultural fields, has middle values of conductivity with vari- able oxygen contents but not direct sewage inputs. We have made some statistical treatment of the data (InVal, for example), but no clear pattern emerged from this treatment due to the high variabil- ity between sites and the low number of taxa. Any other statistical data treatment provides relevant information. Discussion The limited information about midges and their importance for environmental studies There is a very limited information on midges in Mexico. Even less from the Pesquería River where only unpublished degree the- sis of the engineering faculty of the Universidad Nuevo León pro- vide some information. Thus Bermejo (2003) reports some genera from two sites of Pesquería River and Torres (2013) studies the water quality and some biological indicators but identifies only Chironomus gr. plumosus from all the midges collected and uses the family Chironomidae in the biological indices he proposed. If we classify Chironomidae (Diptera) only at family level, their relative importance in taxa richness is not evident. In many cases, the larvae of midges are a major component in taxa number and abundance, especially when some nutrient enrichment or pol- lution is present. It is the case of Pesquería River, where 1/3 of the taxa and close to 50% of the total individuals are Chironomidae (Castro-López et al., 2019b). The study of larvae of Chironomidae is not easy, and it usually takes some time to identify genera or species groups, and the separation of species is not possible in many genera; this is the main reason why such studies are unusual. In addition, several species of the same genera may coexist in a site or even in the same stone (Prat & Garcia-Roger, 2018). The coex- istence of several species may be explained by differences in sub- strate composition or life-cycle characteristics as in Prat & Garcia- Roger, (loc. cit.), but this requires such a work that studies on this topic are the exception in the literature as are those related to func- tional feeding groups, and even more in the Neotropical region (Caleño-Ruiz et al., 2018). For these reasons, it is usual that most of the studies in macroinvertebrates do not use midges at the gen- era level, and few ones use the subfamily level. The lack of keys to classify the midges made more difficult the study of midge lar- vae in Mexico and Latin America in general. Even the most recent keys (Da Silva et al., 2018) are difficult for a non-specialist. Our study reports the actual fauna of midges in the Pesquería River and its relationship with major river basin changes. The results can be used as an indicator of recovery or degradation in further studies. Few papers in Latin America examined the importance of iden- tifying midges at the genera level for a better interpretation of the biodiversity of streams and its relationships with environmental factors (González-Trujillo et al., 2019). The protection of headwa- ters may be the key to the recovery of downstream waters, due to the facility for the drift of insects, including the midges (González- Trujillo, et al., loc. cit.). The use of midges in biomonitoring Most of the literature on bioindicators uses midges at the fam- ily level (or at most at the subfamily). Many researchers as Edwards et al. (2000) and Rossaro et al. (2022b), pointed out the need to use midges at the genera or species level for biomonitoring studies. The revision on the topic (chironomids as bioindicators) made by Nicacio and Juin (2015), does not seem to have con- tributed to an increase of taxonomic studies in midges related to biomonitoring in Mexico or elsewhere in Latin America (except one paper by Molineri et al., 2020). Many of the water quality metrics used for biomonitoring use family or even order as taxonomic level. This is for most of Mexican rivers where people use as the main pollution index the BMWP system (e.g., Pérez-Munguia and López-Pinedo, 2005), including the Pesquería River (Torres-Muñiz, 2013; Castro-López et al., 2019b). Usually this may be enough to characterize the importance of pollution for macroinvertebrates, but doing this (and forgetting the Chironomidae), some important information on rich- ness, diversity, feeding strategies, or pollution tolerance of macroinvertebrate assemblages is missed. Midges are not used at a low taxonomic level for biomonitor- ing to the difficulty and time-consuming task of classifying larvae at genera or species level (even more in Mexico), unless molecular methods may be applied. For example, Ekrem (2019) pointed out that the use of barcoding may improve the usefulness of midge species as bioindicators, but still much work is required to associ- ate a large number of OTUS of midges found in streams to actual species (Failla et al., 2015). For example, in Spain, more than 50% of the taxa of midges present a lack of barcoding results (Murria et al., 2020). The task appears even more difficult in Latin America, where most of the Chironomidae species remain undescribed. Midges, pollution, and landscape The use of midges as indicators of water quality, including eutrophication (mostly in lakes), is common, mostly for their abil- ity to cope with love oxygen water due to the presence of haemo- globin in their body (reviewed by Nicacio & Juen, 2015). In Pesquería River, the red-blood midges are very abundant in both periods (66-71% of individuals). In August, the large Chironomus plumosus (Chironomini) are the dominant species. But this taxa is replaced in February by small Rheotanytarsus;(Tanytarsini), less suited for strong anoxia but still with haemoglobin. This indicated the predominance of organic matter in water and the pollution coming mainly from the non-effective sewage plants or raw sewage in the waters when the river encounters the metropolitan area. In the less polluted sites, several taxa from different subfam- ilies appear as representatives. Our results also suggest that the use of subfamilies and tribes may be, sometimes, useful for biomoni- toring purposes, as did Molineri et al. (2020). We found that the riparian environment is not important, in Pesquería River, for the composition of midges as was in Caro- Borrero and Carmona-Jimenéz (2019), because no correlation [Journal of Entomological and Acarological Research 2023; 55:10861] [page 5] Article No n- co mm er cia l u se on ly [page 6] [Journal of Entomological and Acarological Research 2023; 55:10861] between the values of QBR and the species richness exists. As the river water pollution is so high, the contribution of riparian forests to increase the biodiversity (shade, leaf litter inputs, nutrient filter- ing…) is overpassed by the intensity of river pollution, which only diminishes at the very end of the river after several sites with mod- erate to the low influence of human population in the riparian qual- ity (Castro-López et al., 2019a). Regarding the question of the relevance of landscape in midge composition, we found that only sites with non-modified uses have some characteristic midges, but no differences exist between agri- cultural and urban landscapes, probably because agricultural land- scapes are downstream of the urban sites and part of the pollution coming from urban areas remains in the agricultural landscapes. The change is limited to dominant species, from large red Chironomus to small red Rheotanytarsus, a temporal change relat- ed to the season (August vs. February, dry vs. wet season). This paper is relevant because it characterizes the actual situation of the Pesquería River and may be used as control when further imple- mentation of water purification is done. References ANDERSEN T., CRANSTON P., EPLER J.H., 2013 - Chironomidae of Holartic Region. Keys and diagnoses. Larvae. - Insects’ systematics and evolution. 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